Dysphagia

https://doi.org/10.1007/s00455-018-9920-9 (0123456789().,-volV)(0123456789().,-volV)

ORIGINAL ARTICLE

Changes in Swallowing and Cough Functions Among Stroke Patients

Before and After Tracheostomy Decannulation
Min Kyu Park1 • Sook Joung Lee2

Received: 9 January 2018 / Accepted: 14 June 2018

Ó Springer Science+Business Media, LLC, part of Springer Nature 2018

Abstract
We investigated the functional changes in swallowing and voluntary coughing before and after tracheostomy decannulation
among stroke patients who had undergone a tracheostomy. We also compared these functions between stroke patients who
underwent tracheostomy tube removal and those who did not within 6 months of their stroke. Seventy-seven stroke patients
who had undergone a tracheostomy were enrolled. All patients were evaluated by videofluoroscopic swallowing studies
and a peak flow meter through the oral cavity serially until 6 months after their stroke. During the intensive rehabilitation
period, if a patient satisfied the criteria for tracheostomy tube removal, the tube was removed. The patients were divided
into the ‘decannulated’ group and the ‘non-decannulated’ group according to their tracheostomy tube removal status. In the
decannulated group, swallowing function did not change before and after tracheostomy decannulation; however, cough
function was significantly improved after decannulation. Although both groups exhibited functional improvement in
swallowing and coughing over time, the improvement in the decannulated group was more significant than the
improvement in the non-decannulated group. Our results revealed that stroke patients who had better functional
improvement in swallowing and coughing were more likely to be potential candidates for tracheostomy decannulation.
Stroke patients who recovered from neurogenic dysphagia, they were no longer affected by the mechanical effect of the
tracheostomy tube on swallowing function. This study suggests that if patients show improvement in swallowing and
coughing after their stroke, a multidisciplinary approach to tracheostomy decannulation would be needed to achieve better
rehabilitation outcomes.

Keywords Stroke  Tracheostomy  Deglutition  Cough  Decanulation  Function

Introduction Although early tracheostomy in stroke patients may have

several benefits [2, 3], decannulation of the tracheostomy
After a stroke, patients may lack the ability to protect their tube is preferred if the underlying reason for tracheostomy
airway. When prolonged mechanical ventilation is tube placement has been resolved.
required, a tracheostomy is frequently performed [1]. Although there is currently no protocol for the
decannulation process, previous studies have proposed the
following criteria for tracheal decannulation after traumatic
brain injury [4, 5]: level of consciousness, tracheostomy
& Sook Joung Lee tube capping, respiration, blue dye test, swallowing, and
lsj995414@hanmail.net coughing. Other published guidelines have also revealed
Min Kyu Park that patients should have efficient spontaneous coughing
mkparkdau@gmail.com and subsequent swallowing function [6]. Therefore,
1
Department of Pharmacology and Clinical Pharmacology, according to the findings of previous studies, two important
ChungBuk National University Hospital, Cheongju 28644, factors that are required prior to removal of a tracheostomy
Republic of Korea tube are swallowing and voluntary coughing, which is also
2
Department of Physical Medicine and Rehabilitation, referred to as expectoration [4–7].
Catholic University of Korea, Daejeon St. Mary’s Hospital,
Daejeon 34943, Republic of Korea

123
 M. K. Park, S. J. Lee: Changes in Swallowing and Cough Functions Among Stroke Patients
The effect of a tracheostomy tube on swallowing and
cough functions has been investigated. Several suggested
mechanisms for swallowing dysfunction after tra-
cheostomy include a decrease in laryngeal elevation caused
by tethering of the larynx by the tracheostomy tube [8–10],
direct obstruction of the pharyngeal pathway by the tube
cuff [11], and desensitization of the larynx due to chronic
air diversion [12, 13]. A tracheostomy also affects cough
function. Tracheostomized patients often have difficulty in
initiating the compressive coughing phase, and cough flow
is typically insufficient [14]. Another study demonstrated a
significant increase in peak cough flow (PCF) after tra-
cheostomy tube decannulation [15].
Recent studies have shown that the presence of a tra-
cheostomy tube does not affect the biomechanics or kine-
matics of swallowing [16–18]. However, these studies were
performed in patients who had sufficient swallowing and
cough functions to safely remove the tracheostomy tube at
the subacute stage or chronic stage. In addition, the
enrolled patients in these studies had various etiologies that
required tracheostomy tube placement, including stroke,
vocal cord palsy, neuromuscular disorder, sepsis, and sleep
apnea.
Few studies have evaluated functional changes in stroke
patients before and after tracheostomy tube removal. Cur-
rent studies have suggested a pattern of recovery after
stroke with the timing of specific intervention strategies,
which include multidisciplinary rehabilitation therapy [19].
As stroke shows various clinical manifestations and
recovery processes, swallowing and cough functions also
change and improve after a stroke over time. In addition,
the mechanical effect of a tracheostomy tube on swallow-
ing and cough functions differ depending on the time after
stroke onset, because neurogenic dysphagia after stroke
recovers over time. If a patient is a potential candidate for
tracheostomy tube removal, personalized, intensive
approaches are needed for tracheostomy decannulation.
The aims of this study were to investigate the functional
changes in swallowing and voluntary coughing before and
after tracheostomy decannulation in stroke patients. We
also compared these functional statuses between stroke
patients who underwent tracheostomy tube removal and
those who did not within 6 months of their stroke. In
addition, we evaluated various functional statuses other
than swallowing and cough function, such as cognition and
activities of daily living.
123
Methods
Subjects
This study was designed as an observational prospective
study and was conducted in the rehabilitation center of a
university hospital, specifically a regional cerebrovascular
center. Subacute stroke patients who had undergone a
tracheostomy between March 2015 and December 2016
were enrolled. Patients who had previous strokes, a history
of head or neck cancer, neuromuscular disease, or a poor
general condition that would not permit the videofluoro-
scopic swallowing studies (VFSS) were excluded. All
patients were in the subacute period of stroke and received
personalized, intensive rehabilitation including physio-
therapy, occupational therapy, swallowing therapy, and
speech therapy.
The study protocol was approved by the institutional
review board, and all participants provided written
informed consent. (Dong-A University Hospital, IRB No:
15-156).
Tracheostomy Decannulation
The criteria for tracheostomy tube removal were adopted
from previous studies [4, 5]: alert mental status, good
respiratory function; anatomically intact upper airway as
determined by laryngoscopy; including the ability to tol-
erate tracheostomy tube capping; reduced tracheal secre-
tions; and intact swallowing and cough function. Patients
who had undergone tracheostomy, had the ability to tol-
erate tube capping for 48 h and had the capacity to
expectorate without assistance were eligible for tra-
cheostomy tube removal. Tracheostomy decannulation was
performed with consultation from the Department of
Otorhinolaryngology. No patients required reinsertion of
their tracheostomy tube after removal. The tracheostomy
tubes were not downsized prior to tube decannulation.
Evaluation
All patients underwent VFSS and peak flow meter evalu-
ations through the oral cavity to measure PCF every 2 or
4 weeks according to their medical and neurological con-
dition. If patients satisfied the criteria for tracheostomy
tube removal, the tracheostomy tube was removed. VFSS
and PCF evaluations were performed within 7 days before
and after tracheostomy decannulation. In patients who were
not able to have their tracheostomy tube removed, these
evaluations were serially performed within 6 months of
their stroke. The patients were divided into a ‘decannu-
lated’ group and a ‘non-decannulated’ group according to
M. K. Park, S. J. Lee: Changes in Swallowing and Cough Functions Among Stroke Patients
their tracheostomy removal status. All test procedures were
recorded, and the findings were analyzed by three experi-
enced physiatrists.
Functional Evaluations
Swallowing Function
Swallowing function was evaluated using the functional
dysphagia scale (FDS) and penetration aspiration scale
(PAS) based on the results of the VFSS. VFSS were per-
formed with the patients in a sitting position to allow a
lateral view. A modified version of the protocol from a
study performed by Logemann was employed [20]. All
patients received individualized feeding therapy based on
the results of the VFSS.
The FDS was developed to quantify the severity of
dysphagia; it correlates well with the American Speech-
Language-Hearing Association national outcome mea-
surement system criteria [21]. The FDS consists of 11
items with weighted values that represent 4 types of oral
functions (lip closure, bolus formation, residues in oral
cavity, and oral transit time) and 7 types of pharyngeal
functions (triggering of pharyngeal swallow, laryngeal
elevation and epiglottic closure, nasal penetration, residue
in valleculae, residue in pyriformis sinus, coating of pha-
ryngeal wall after swallowing, and pharyngeal transit time)
that can be observed using VFSS. To determine the dif-
ferences in the parameters related to a tracheostomy tube,
the patients’ FDS scores were divided into subsections and
analyzed.
The PAS evaluates airway invasions [22] and has a
maximum score of 8 points. Scores are determined pri-
marily based on the depth to which material passes into the
airway and whether material entering the airway can be
expelled. The penetration category corresponds to level 5
on the scale, and levels 6–8 correspond to laryngo-tracheal
aspiration. A PAS score of 8 indicates that material enters
the airway, passes below the vocal folds, and no effort is
made to eject the material.
Voluntary Cough Function
PCF was used to measure voluntary coughing ability,
which was assessed by having patients cough as forcefully
as possible through a peak flow meter. Prior to testing,
patients were allowed to use the peak flow meter several
times to become accustomed to the test. For PCF testing,
the opening of the tracheostomy tube was temporarily
occluded during expiration, and the patient’s lips were
placed tightly around a mouthpiece. A maximum of three
attempts were used for the analysis. PCF is the primary
parameter in assessing voluntary coughing efficacy;
numerous studies have employed this parameter as a vol-
untary cough measurement tool [23–25].
Parameters that can affect functional outcomes, includ-
ing initial stroke characteristics, Korean version of Mini-
Mental State Examination (K-MMSE) scores, Korean
version of the modified Barthel Index (K-MBI) scores, and
the presence of aphasia and neglect, were also evaluated.
Statistical Analysis
SPSS 21.0 for Windows was used for statistical analysis.
Student’s t test and the Chi-square test were performed to
compare the two groups, namely, the group of patients who
were eligible for tracheostomy tube removal within
6 months after their stroke and the group of patients who
were not. A paired t-test or repeated-measure analysis of
variance (ANOVA) was used to compare data obtained
serially in each group. A p value of less than 0.05 was
considered statistically significant. Post hoc analysis was
performed using the Tukey honestly significant difference
test if there was a significant effect using the repeated-
measures ANOVA.
Results
One hundred and one patients with a tracheostomy tube
were enrolled from March 2015 to December 2016. Among
these patients, 13 were excluded, and 11 were lost to fol-
low-up. Seventy-seven patients satisfied the inclusion cri-
teria and were analyzed in this study. Most patients (63
patients, 81.8%) were transferred from the Department of
Neurosurgery due to a large amount of intracerebral hem-
orrhage (ICH), intravenous hemorrhage (IVH), malignant
ischemic infarction with hemorrhage transformation, or
malignant ischemic infarction with severe brain edema that
showed midline shifting and required a craniectomy. Tra-
cheostomy was performed 10.9 ± 6.1 days after the onset
of stroke. The most common cause of tracheostomy was
failure of ventilator weaning. Of the included patients, 35
were eligible for tracheostomy tube removal within
6 months of their stroke.
Table 1 lists the baseline demographic characteristics of
the tracheostomized patients. At the onset of stroke, the
patients in the decannulated group were significantly
younger than the patients in the non-decannulated group
(the patients who were ineligible for tracheostomy tube
removal within 6 months of their stroke). The initial stroke
characteristics, including ischemic or hemorrhagic stroke
and supratentorial or infratentorial stroke, and the initial
National Institutes of Health Stroke Scale (NIHSS) scores,
were not significantly different between these two groups.
In addition, the initial functional evaluations, including
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 M. K. Park, S. J. Lee: Changes in Swallowing and Cough Functions Among Stroke Patients

Table 1 Baseline demographic characteristics of tracheostomy patients

Decannulated group (n = 35) Non-decannulated group (n = 42) p value

Age 50.6 ± 11.0 63.7 ± 10.1 0.03*

Gender (male/female) 20/15 23/19 0.087
Days from stroke onset 27.4 ± 5.9 31.8 ± 11.4 0.158
Duration from stroke onset to tracheostomy (days) 10.1 ± 5.0 12.6 ± 5.5 0.113
Stroke character
Ischemic/hemorrhagic 11/24 14/28 0.071
Operation (craniectomy, craniotomy) 7/19 20/17 0.416
Supratentorial/infratentorial 22/13 19/23 0.57
Rt/Lt/bilateral 8/12/15 15/12/15
Initial NIHSS 21.4 ± 6.2 23.2 ± 4.4 0.471
Initial mRS 4.7 ± 2.4 4.8 ± 2.1 0.128
Neglect (yes/no) 11/24 20/22 0.081
Aphasia (yes/no) 13/22 16/26 0.283
FDS total (0–100) 48.2 ± 35.1 52.9 ± 28.7 0.352
FDS oral (0–38) 10.2 ± 7.3 15.1 ± 8.2 0.087
FDS pharyngeal (0–62) 34.7 ± 15.3 46.5 ± 20.2 0.139
PAS 7.1 ± 3.4 7.8 ± 2.9 0.661
PCF (L/min) 57.1 ± 29.8à 51.5 ± 32.7§ 0.597
K-MBI (0–100) 11.8 ± 10.5 5.7 ± 10.7 0.073
K-MMSE (0–30) 4.6 ± 12.1 1.9 ± 9.3 0.258
Values are the number or mean ± SD
NIHSS National Institute of Health Stroke scale, MRS modified Rankin Scale, FDS functional dysphagia scale, PAS penetration aspiration scale,
PCF peak cough flow, K-MBI Korean-version of the modified Barthel index, K-MMSE Korean-version of the mini-mental state examination
*p \ 0.05 by the Student t-test
à
Only in 14 patients
§
Only in 17 patients

swallowing, coughing, cognition, and activities of daily
living, showed no statistically significant between-group
differences.
Figure 1 shows the changes in swallowing functions
among patients who were eligible for tracheostomy tube
removal (decannulated group) at initial evaluation and
before and after tracheostomy decannulation, according to
the time. Patients in the decannulated group demonstrated
significant improvements in swallowing function over
time. Post hoc analysis showed that based on the FDS
scores, significant improvement in swallowing function
was achieved from baseline to before tracheostomy tube
removal, and from baseline to after tracheostomy tube
removal; however, no significant changes were observed
when comparing swallowing function between before and
after tracheostomy decannulation (Fig. 1a). However,
based on the PAS scores, significant improvement was
observed between before and after the tracheostomy
decannulation (Fig. 1b). Cough function also showed sig-
nificant improvement over time, and the post hoc test
revealed that cough function was significantly improved
after tracheostomy tube removal (Fig. 2).
In the decannulated group, the shortest duration of tra-
cheostomy time was 37 days, which was achieved by a
31-year-old man with a hypertensive ICH in the basal
ganglia and IVH. The lowest PCF score before tra-
cheostomy tube removal of 112 L/min was observed in a
56-year-old male patient with malignant middle cerebral
artery (MCA) infarction who had undergone a craniec-
tomy. Among the decannulated patients, 31.4% required a
limited diet consisting of soft blended diet and fluid with a
thickener (viscosity range 351–1750 cP) [26] due to the
risk of aspiration immediately prior to tracheostomy
decannulation.
Table 2 shows the various functional changes in each
group from the baseline evaluation to immediately before
tracheostomy tube removal in the decannulated group and
6 months after tracheostomy tube removal in the non-de-
cannulated group. In the non-decannulated group, which
included patients who could not undergo tracheostomy
tube removal, functional evaluations at baseline and at
6 months after the onset of stroke were compared. Both
groups showed improvement in most functional measure-
ments, including swallowing, coughing, cognitive function,

123
M. K. Park, S. J. Lee: Changes in Swallowing and Cough Functions Among Stroke Patients
Fig. 1 Changes in swallowing function over time among patients who
were eligible for tracheostomy tube removal. Patients in the
decannulated group demonstrated significant improvements in swal-
lowing function over time. Post hoc analysis showed that based on the
FDS scores, significant improvement in swallowing function was
achieved from baseline to before tracheostomy tube removal, and
from baseline to after tracheostomy tube removal; however, no
significant changes were observed between before and after
and activities of daily living. However, patients in the non-
decannulated group showed no improvements in the PCF
and PAS scores.
The initial functional evaluations for both groups
showed no significant differences. When we compared
these two groups immediately prior to tracheostomy
decannulation in the decannulated group and 6 months
after the onset of stroke in the non-decannulated group, the
patients in the decannulated group achieved significantly
higher FDS, PAS, PCF, MBI and MMSE scores. In the
decannulated group, all patients could tolerate an oral diet
(24 received a normal regular diet and 11 received a lim-
ited diet). However, 38.1% (n = 16) of patients in the non-
decannulated group could not consume their diet orally.
When comparing the changes between the two groups
(Table 3), the decannulated group had significantly higher
scores than the non-decannulated group for swallowing and
coughing functions. The decannulated group also achieved
higher activities of daily living (ADL) scores and showed
greater cognitive function improvements than the non-de-
cannulated group.
Complications related to tracheostomy decannulation,
including arterial desaturation, tracheal stenosis, granu-
loma, and pneumonia, did not occur in this population.
None of the patients required reinsertion of a tracheostomy
tracheostomy decannulation (a). Based on the PAS scores, significant
improvement was observed between before and after the tra-
cheostomy decannulation (b). *p \ 0.05 by ANOVA. Post hoc t-
test: a p \ 0.017 indicating a significant difference between initial
and before tracheostomy decannulation. b p \ 0.017 indicating a
significant difference between initial and after tracheostomy decannu-
lation. c p \ 0.017 indicating a significant difference between before
and after tracheostomy decannulation
tube after removal. The reasons for failure to remove a
tracheostomy tube in the non-decannulated group (n = 42)
included uncooperative mental status (n = 20, 47.6%), lack
of coughing ability resulting in failure to expectorate spu-
tum or post-swallowing residue (n = 14, 33.3%), large
amounts of secretion, and failure to deflate the tra-
cheostomy tube cuff (n = 18, 42.9%). Of the patients in the
non-decannulated group, 16 (38.1%) could not restore oral
swallowing function; thus, a percutaneous endoscopic
gastrostomy tube was inserted. In addition, 7 patients had a
recurrent stroke.
Discussion
This study aimed to demonstrate functional changes in
swallowing and voluntary coughing among stroke patients
before and after tracheostomy decannulation. When these
functions were compared before and after tracheostomy
decannulation, our results revealed that swallowing func-
tion did not change at tracheostomy tube removal, whereas
cough function was significantly increased after tra-
cheostomy decannulation.
Most stroke patients with a tracheostomy tube showed
various functional improvements (including not only
123
 M. K. Park, S. J. Lee: Changes in Swallowing and Cough Functions Among Stroke Patients
Fig. 2 Changes in cough function over time among patients in the
decannulated group. The PCF scores showed significant improvement
in cough function over time, and post hoc tests revealed that cough
function was significantly improved after tracheostomy tube removal.
*p \ 0.05 by ANOVA. Post hoc t-test; a p \ 0.017 indicating a
significant difference between initial and before tracheostomy
decannulation. b p \ 0.017 indicating a significant difference
between initial and after tracheostomy decannulation. c p \ 0.017
indicating a significant difference between before and after tra-
cheostomy decannulation
swallowing and coughing but also cognitive function and
ADLs) over time regardless of whether she/he satisfied the
criteria for tracheostomy tube removal. However, the
functional improvement in patients who were eligible for
tracheostomy tube removal (decannulated group) was sig-
nificantly higher than the improvement among patients in
the non-decannulated group. Patients who were younger at
the onset of stroke and had better functional improvement
and were more likely to be considered as a potential can-
didate for tracheostomy decannulation. The initial stroke
characteristics were not related to the ability to perform
tracheostomy decannulation.
Functional Changes in Swallowing and Coughing
According to the Evaluation Time
Swallowing functions before and after tracheostomy
decannulation did not significantly differ in this study.
Previous studies have demonstrated that tracheostomy
tubes do not affect the biomechanics and kinematics of
swallowing function [16–18]. However, other studies have
revealed the interference of tracheostomy on swallowing
function due to a decrease in laryngeal elevation as a result
of tethering of the larynx by the tracheostomy tube [8, 9],
123
direct obstruction of the pharyngeal pathway by the tube
cuff [11], and desensitization of the larynx.
The swallowing evaluation time after stroke onset was
an important factor in the different effect from a tra-
cheostomy tube on swallowing function. The acute phase
of stroke patients involved neurogenic dysphagia and
pharyngeal weakness; thus, the mechanical effects of a
tracheostomy tube may negatively affect swallowing
function. However, it appeared that stroke patients who had
recovered from neurogenic dysphagia or displayed
improvements in pharyngeal weakness were not affected
by the mechanical effects of the tracheostomy tube on
swallowing function. In previous studies [16–18], enrolled
patients were in the chronic stages of their dysphagia
symptoms or have recovered from neurogenic dysphagia;
thus, swallowing function was not changed before and after
tracheostomy tube removal.
In contrast, cough function after tracheostomy
decannulation significantly increased, which is consistent
with a previous study [14, 15]. It appears that the
mechanical effect of a tracheostomy tube inhibits maximal
cough function regardless of whether a patient’s swallow-
ing function has recovered. Because the tracheostomy tube
is positioned in the way of cough output, thus, it acts as a
barrier and can generate airway resistance against maximal
cough function.
Relation Between Swallowing and Cough
for Removal of the Tracheostomy Tube
Several studies reported that swallowing and coughing are
important criteria for tracheal decannulation and are clo-
sely connected [4–6, 27]. However, safe decannulation was
achieved in stroke patients who did not achieve normal
functional status for both swallowing and coughing. Our
previous study also indicated a discrepancy between
swallowing and coughing in stroke patients based on their
stroke lesion [28].
In this study, 31.4% of patients required a restricted
dietary formula due to the risk of aspiration prior to tra-
cheostomy decannulation. Even though patient’s swal-
lowing function was not completely recovered, if the
patient’s cough function was appropriate, with expectora-
tion of post-swallowing residue, the patient was able to
undergo their tracheostomy tube removal.
Mckim [15] and Winck [29] reported that PCF values
greater than 160 L/min indicate successful decannulation.
However, the mean PCF values prior to tracheostomy tube
removal were 129.1 ± 28.1 L/min in our study, and 78%
of patients obtained PCF values lower than 160 L/min.
These patients showed no post-swallowing residue and had
a low risk of pharyngeal aspiration; thus, they were able to
have their tracheostomy tubes removed despite low PCF
M. K. Park, S. J. Lee: Changes in Swallowing and Cough Functions Among Stroke Patients

Table 2 Functional changes between groups

Decannulated group (n = 35) p value Non-decannulated group (n = 42) p value p value
Initial Before tracheostomy Initial 6 months after
removal onset

Days from stroke onset 27.4 ± 5.9 82.6 ± 13.2 – 31.8 ± 11.4 183.7 ± 21.8 – –
Tracheostomized period 12.5 ± 4.8 67.7 ± 22.7 – 15.8 ± 8.1 173.6 ± 33.8 – –
(days)
mRS 4.7 ± 2.4 2.8 ± 1.7 0.003* 4.8 ± 2.1 3.7 ± 2.5 0.02* 0.072 
FDS total (0–100) 48.2 ± 35.1 15.9 ± 8.5 0.001* 52.9 ± 28.7 33.3 ± 12.4 0.04* 0.001 
FDS oral (0–38) 10.2 ± 7.3 2.9 ± 4.3 0.001* 15.1 ± 8.2 10.1 ± 5.5 0.001* 0.001 
FDS pharyngeal (0–62) 34.7 ± 15.3 13.0 ± 10.1 0.02* 46.5 ± 20.2 32.4 ± 13.1 0.031* 0.001 
PAS 7.1 ± 3.4 3.7 ± 2.9 0.001* 7.8 ± 2.9 6.4 ± 3.1 0.06 0.002 
à k
PCF (L/min) 57.1 ± 29.8 129.1 ± 28.1 0.001* 51.5 ± 32.7 §
60.8 ± 11.8 0.184 0.001 
Diet (NRD/LD/nonoral) 0/0/35 24/11/0 – 0/0/42 0/26/16 –
K-MBI (0–100) 11.8 ± 10.5 56.4 ± 30.1 0.001* 5.7 ± 10.7 34.9 ± 18.2 0.037* 0.001 
K-MMSE (0-30) 4.6 ± 12.1 21.8 ± 12.8 0.001* 1.9 ± 9.3 7.8 ± 5.1 0.001* 0.001 
Values are the number or mean ± SD
FDS functional dysphagia scale, PAS penetration aspiration scale, PCF peak cough flow, NRD normal regular diet, LD limited diet, K-MBI
Korean-version of the modified Barthel index, K-MMSE Korean-version of the mini-mental state examination
*p \ 0.05 by the Pared t-test in each group
 
p \ 0.05 by Student t-test, the two groups were compared immediately before tracheostomy decannulation in ‘‘decannulated’’ group patients
and 6 months after the onset of stroke in ‘‘non-decannulated’’ group
à
Only in 14 patients
§
Only in 17 patients
k
Only in 28 patients

Table 3 Comparison of functional changes between groups before tracheostomy removal

Changes Decannulated group (n = 35) Non-decannulated group (n = 42) p value
Changes between initial evaluation and before tracheostomy Changes between initial evaluation and 6 months
remoal after onset

DFDS total 30.2 ± 17.5 23.3 ± 15.8 0.001*

DFDS oral 7.1 ± 5.5 5.4 ± 2.8 0.07
DFDS 24.7 ± 11.5 16.3 ± 12.7 0.01*
pharyngeal
DPAS 3.6 ± 2.9 1.4 ± 1.9 0.002*
DPCF 80.9 ± 32.4 26.1 ± 11.7 0.02*
DK-MBI 52.1 ± 26.3 31.8 ± 11.9 0.03*
DK-MMSE 18.5 ± 12.7 7.1 ± 5.4 0.001*
Values are the number or mean ± SD
FDS functional dysphagia scale, PAS penetration aspiration scale, PCF peak cough flow, K-MBI Korean-version of the modified Barthel index,
K-MMSE Korean-version of mini-mental status exam
*p \ 0.05 by Student’s t-test

values. In contrast, patients who had PCF values above 160
L/min but showed silent aspiration on VFSS were not able
to have their tracheostomy tubes removed, particularly
those with infratentorial lesions.
Thus, we would like to suggest that fully intact cough
and swallowing function are not indications for tra-
cheostomy tube removal. As previously described, various
functions appear to be related to the ability to remove a
patient’s tracheostomy tube, and a multidisciplinary

123
 M. K. Park, S. J. Lee: Changes in Swallowing and Cough Functions Among Stroke Patients
individual approach is needed to determine the earliest
possible time at which the tube can be removed in stroke
patients.
Multidisciplinary Approach to Tracheostomy
Decannulation After a Stroke
In this study, when comparing the functional changes
between two groups, the decannulated group had signifi-
cantly higher scores than the non-decannulated group for
swallowing, coughing, cognition, and ADL functions.
Previous studies have emphasized that a multidisciplinary
approach to post-tracheostomy care is important for the
safe removal of a tracheostomy tube [6, 15, 27, 30].
Decannulation is a complex and multidisciplinary process
that is affected by various factors. Our results indicated that
various functions could affect tracheostomy tube removal
in stroke patients. In this study, the functional status of the
patient, including not only swallowing and cough functions
but also ADL and cognitive functions, was evaluated; these
functions could affect the safety of tracheostomy tube
removal. This study was the first to evaluate the general-
ized functional status in stroke patients with tracheostomy
after decannulation.
The removal of a tracheostomy tube is an important
rehabilitation goal but cannot always be performed [31].
Only a few studies have focused on post-tracheostomy care
and functional evaluations; thus, post-tracheostomy care is
often neglected in an otherwise thorough evaluation of
individual tracheostomy decannulation [30, 32]. Because
most functions including swallowing and coughing, are
shown to rapidly recover within 6 months after stroke, our
results suggest that if a patient shows improvement in
swallowing and cough functions after stroke in this period,
a multidisciplinary approach to achieve the earliest possi-
ble time of tracheostomy decannulation is required for
better rehabilitation outcomes. [19, 33].
Strengths and Limitations
To our knowledge, this study was the first to demonstrate
various functional relationships before and after tra-
cheostomy tube removal in patients with stroke. Only
patients with subacute stage stroke who had undergone
tracheostomy tube placement were enrolled.
However, this study has several limitations, particularly
the low number of enrolled patients, and low number of
subjects who completed the baseline PCF evaluation, par-
ticularly in the non-decannulated group, as after stroke,
patients with aphasia, apraxia or cognitive impairment
could not conduct PCF test according to the examiner’s
command. Although we attempted to classify the patients
according to their stroke lesions, most patients had a
123
malignant MCA infarction or large ICH, including IVH,
and had both supratentorial and infratentorial lesions. As a
result, we were unable to divide the groups by distinct
stroke lesions. Furthermore, the times at which both groups
were compared differed; the decannulated group was
evaluated before tracheostomy removal, whereas the non-
decannulated group was evaluated 6 months after stroke.
However, maximal recovery from stroke occurs within
6 months, which explains why we evaluated functional
measures at 6 months in the decannulated group. We did
not perform the blue dye test, which was one of the
important factors of tracheostomy tube removal.
Conclusion
Our results revealed that swallowing function did not
change before and after tracheostomy decannulation;
however, cough function was significantly improved after
decannulation. Stroke patients who recovered from neu-
rogenic dysphagia, they were no longer affected by the
mechanical effect of the tracheostomy tube on swallowing
function. In addition, stroke patients who had better func-
tional improvement in swallowing and coughing were
more likely to be potential candidates for tracheostomy
decannulation. Thus, we suggest that if patients show
improvement in swallowing and cough functions after their
stroke, a multidisciplinary approach to tracheostomy
decannulation will be needed to achieve better rehabilita-
tion outcomes.
Funding This study was partially supported by the Dong-A Univer-
sity research fund.
Compliance with Ethical Standards
Conflict of interest The authors declare that they have no conflict of
interest.
Ethical Approval This article does not contain any studies with human
participants performed by any of the authors.
Informed Consent Informed consent was obtained from all individual
participants included in the study.
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Min Kyu Park MD, PhD
Sook Joung Lee MD, PhD
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